Multicellular Magnetotactic Prokaryotes Research Articles

Novel species and expanded distribution of ellipsoidal multicellular magnetotactic prokaryotes.

Multicellular magnetotactic prokaryotes (MMPs) are a peculiar group of magnetotactic bacteria, each comprising approximately 10-100 cells of the same phylotype. Two morphotypes of MMP have been identified, including several species of globally distributed spherical mulberry-like MMPs (s-MMPs), and two species of ellipsoidal pineapple-like MMPs (e-MMPs) from China (Qingdao and Rongcheng cities). We recently collected e-MMPs from Mediterranean Sea sediments (Six-Fours-les-Plages) and Drummond Island, in the South China Sea. Phylogenetic analysis revealed that the MMPs from Six-Fours-les-Plages and the previously reported e-MMP Candidatus Magnetananas rongchenensis have 98.5% sequence identity and are the same species, while the MMPs from Drummond Island appear to be a novel species, having > 7.1% sequence divergence from the most closely related e-MMP, Candidatus Magnetananas tsingtaoensis. Identification of the novel species expands the distribution of e-MMPs to Tropical Zone. Comparison of nine physical and chemical parameters revealed that sand grain size and the content of inorganic nitrogen (nitrate, ammonium and nitrite) in the sediments from Rongcheng City and Six-Fours-les-Plages were similar, and lower than found for sediments from the other two sampling sites. The results of the study reveal broad diversity and wide distribution of e-MMPs.

青岛太平湾潮间带趋磁细菌多样性

PDF HTML阅读 XML下载 导出引用 引用提醒 青岛太平湾潮间带趋磁细菌多样性 DOI: 10.5846/stxb201412012380 作者: 作者单位: 中国科学院海洋研究所 海洋生态与环境科学重点实验室;中国科学院大学,中国科学院海洋研究所 海洋生态与环境科学重点实验室,中国科学院海洋研究所 海洋生态与环境科学重点实验室,中国科学院海洋研究所 海洋生态与环境科学重点实验室,中国科学院海洋研究所 海洋生态与环境科学重点实验室,中国科学院海洋研究所 海洋生态与环境科学重点实验室,中国科学院海洋研究所 海洋生态与环境科学重点实验室,中国科学院海洋研究所 海洋生态与环境科学重点实验室 作者简介: 通讯作者: 中图分类号: 基金项目: 国家自然科学基金项目（41276170，41206150，41330962）；国际海域资源调查与开发“十二五”项目（深海（微）生物资源勘探与资源潜力评价）（任务书编号：DY125-15-R-03） Diversity of magnetotactic bacteria in the intertidal zone of Taiping Bay, Qingdao Author: Affiliation: Key Laboratory of Marine Ecology and Environmental Sciences,Institute of Oceanology,Chinese Academy of Sciences; University of Chinese Academy of Sciences,Key Laboratory of Marine Ecology and Environmental Sciences,Institute of Oceanology,Chinese Academy of Sciences,Key Laboratory of Marine Ecology and Environmental Sciences,Institute of Oceanology,Chinese Academy of Sciences,Key Laboratory of Marine Ecology and Environmental Sciences,Institute of Oceanology,Chinese Academy of Sciences,Key Laboratory of Marine Ecology and Environmental Sciences,Institute of Oceanology,Chinese Academy of Sciences,Key Laboratory of Marine Ecology and Environmental Sciences,Institute of Oceanology,Chinese Academy of Sciences,Key Laboratory of Marine Ecology and Environmental Sciences,Institute of Oceanology,Chinese Academy of Sciences,Key Laboratory of Marine Ecology and Environmental Sciences,Institute of Oceanology,Chinese Academy of Sciences Fund Project: 摘要 | 图/表 | 访问统计 | 参考文献 | 相似文献 | 引证文献 | 资源附件 | 文章评论 摘要:在青岛太平湾潮间带沉积物中发现了一定量的海洋趋磁细菌，最大丰度可达350个/cm3。透射电镜观察发现该区域趋磁细菌均为趋磁球菌。磁小体个体形状单一，皆是立方体状；磁小体排列方式多样，以链状排列为主，包括单链、双链与多链，也有少数成簇排列。EDS结果表明，磁小体成分为四氧化三铁。据估算，趋磁细菌的铁元素含量（干重）范围在0.40%-6.91%之间，平均为2.19%。通过16S rRNA基因文库的构建与测序得到了47个趋磁细菌序列，分属13个OTU。系统发育分析结果表明，它们都属于α-变形菌纲，其中9个OTU与已知最相似序列的相似性低于97%，有5个OTU与已知最相似序列的相似性低于93%，可能代表了趋磁细菌的9个新种、5个新属，说明该区域潜在的微生物新种质资源十分可观。 Abstract:Magnetotactic bacteria (MTB) are gram-negative motile prokaryotes that produce magnetosomes and can orient and migrate along the geomagnetic lines of force. They are ubiquitous in sediments and stratified water columns, distributed predominantly in the oxic-anoxic transition zone (OATZ). MTB comprise several morphological types, including cocci, rods, vibrios, spirilla, and multicellular magnetotactic prokaryotes. Usually, cocci are the dominant morphology. Variable phylogenetic relatedness of MTB has been confirmed on the basis of 16S rRNA genes. MTB can biomineralize iron oxide and/or iron sulfide magnetosomes. In most MTB, magnetosomes are organized in chain(s). In this study, we found a certain amount of MTB in the intertidal zone of Taiping Bay, Qingdao City, where the maximum abundance reaches up to 350 ind./cm3. Transmission electron microscopy revealed that all the MTB were magnetotactic cocci, with a size of (2.23±0.69) μm×(1.84±0.47) μm and the width/length ratio of 0.87±0.10 (n=21). Fifty-four percent of the MTB contained two chains of magnetosomes, eighteen percent with one chain, fourteen percent with more than two chains and fourteen percent with cluster. All of these magnetosomes were prismatic mineral crystals. There were 7-43 (mean=18,n=21) magnetosomes in a cell and the volume of magnetosomes varied between 2.71×105 nm3 and 1.63×106 nm3. Assuming that all the magnetosomes were magnetite, the percentage of Fe in MTB was 0.40%-6.91% (average 2.19%) and per square kilometer of intertidal zone produced 1.92 kg magnetite every year. This suggests that MTB may play an important role in the iron biogeochemical cycle in this area. Additionally, according to the statistics for each magnetotactic bacterium, we observed that the mass of magnetosome increased with the increasing mass of MTB (r=0.637,P=0.002 < 0.05). Phylogenetic analysis based on 16S rRNA gene sequences revealed that 47 sequences of MTB belonged to 13 OTUs (XCQD1-18, 1-2, 1-19, 51, 81, 6, 2-2, 4-20, 34, 2-23, 53, 130, 1-21) and affiliated to Alphaproteobacteria. OTU XCQD1-18 containing 23 sequences had the highest dominance index (48.93%). In addition, 6, 5, 2, 2, 2 sequences belonged to OTU XCQD2-2, XCQD1-21, XCQD1-2, XCQD2-23, XCQD130, respectively. The other OTUs had only one sequence. Shannon's diversity index H' of MTB in Taiping Bay was 2.64nit, and Species Evenness J' was 0.71. Nine OTUs (XCQD 1-18, 1-2, 1-19, 81, 6, 4-20, 34, 2-23, 53) shared less than 97% 16S rRNA gene sequence similarity with the nearest known sequences, in which, five OTUs (XCQD 81, 4-20, 4, 2-23, 53) shared lower than 93%. It suggested that they represented 9 new species and 5 novel genera. Our results indicate that there were substantial potential microorganism resources in Taiping Bay. Compared to the MTB community in Huiquan Bay, a bay adjacent to Taiping Bay, here were two MTB OTUs discovered both in Taiping Bay and Huiquan Bay. Two MTB OTUs were shared. Jaccard similarity coefficient was 0.1053, indicating that although the two bays were close to each other, the MTB communities showed great differences. Comparison of the features of MTB in Taiping Bay with two French Mediterranean coasts, Six-Fours-les-Plages and Gulf of Fos, revealed that environmental factors may have a great influence on the diversity of MTB. It is assumed that community succession, seasonal variation, and environmental distinction may contribute to the low similarity between the MTB communities and features of different intertidal areas. Our results imply that further investigation on MTB in terms of their diversity is required. 参考文献 相似文献 引证文献

Photokinesis is magnetic field dependent in the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis.

Candidatus Magnetoglobus multicellularis is a spherical, multicellular, magnetotactic prokaryote (MMP) composed of 10-40 genetically-identical, Gram-negative cells. It is known that monochromatic light of low intensity influences its average swimming velocity, being higher for red light (628 nm) and lower for green light (517 nm). In this study, we determined the effect of light of different wavelengths and intensities on the swimming velocity of Ca. Magnetoglobus multicellularis under different magnetic field intensities. The swimming velocities of several organisms exposed to blue light (469 nm), green light (517 nm) and red light (628 nm) with intensities ranging from 0.36 to 3.68 Wm(-2) were recorded under magnetic field intensities ranging from 0.26 to 1.47 Oe. Our results showed that MMPs exposed to green light display consistently lower average swimming velocities compared to other wavelengths of light. We also show for the first time that photokinesis in Ca. Magnetoglobus multicellularis is dependent on the magnetic field being applied. The relationship between light wavelength and intensity and magnetic field strength and swimming velocity in this MMP is therefore complex. Although the mechanism for the observed behaviour is not completely understood, a flavin-containing chromophore may be involved.

Temporal distributions and environmental adaptations of two types of multicellular magnetotactic prokaryote in the sediments of Lake Yuehu, China.

Two morphotypes (spherical and ellipsoidal) of multicellular magnetotactic prokaryotes (MMPs) have been reported from the sediments of Lake Yuehu, China. Here, their temporal distributions and their relationships with biogeochemical parameters are studied. Samples were collected at approximately 2-week intervals from two sites (A and B) during the period September 2012 to December 2013. The abundance of MMPs was high in summer and autumn, but low in winter and spring. Furthermore, the peaks in the numbers of the two types of MMPs were sequential, with the highest concentration of the spherical MMPs occurring prior to that of the ellipsoidal MMPs. This may be related to different optimal growth temperatures for the two types. Although the two types of MMP coexisted at both sites, their numbers were different; at most times, spherical MMPs dominated at site A, whereas ellipsoidal MMPs dominated at site B. Geochemical analysis revealed that the environmental conditions at site A varied more than at site B. Compared with the widely distributed spherical MMPs, ellipsoidal MMPs seemed to prefer more stable habitats. This is the first report of the temporal distribution of ellipsoidal MMPs in sediments, suggesting that their environmental adaptations differ from those of spherical MMPs.

Single-cell genomics reveals potential for magnetite and greigite biomineralization in an uncultivated multicellular magnetotactic prokaryote.

For magnetic orientation, magnetotactic bacteria biosynthesize magnetosomes, which consist of membrane-enveloped magnetic nanocrystals of either magnetite (Fe3 O4 ) or greigite (Fe3 S4 ). While magnetite formation is increasingly well understood, much less is known about the genetic control of greigite biomineralization. Recently, two related yet distinct sets of magnetosome genes were discovered in a cultivated magnetotactic deltaproteobacterium capable of synthesizing either magnetite or greigite, or both minerals. This led to the conclusion that greigite and magnetite magnetosomes are synthesized by separate biomineralization pathways. Although magnetosomes of both mineral types co-occurred in uncultured multicellular magnetotactic prokaryotes (MMPs), so far only one type of magnetosome genes could be identified in the available genome data. The MMP Candidatus Magnetomorum strain HK-1 from coastal tidal sand flats of the North Sea (Germany) was analysed by a targeted single-cell approach. The draft genome assembly resulted in a size of 14.3 Mb and an estimated completeness of 95%. In addition to genomic features consistent with a sulfate-reducing lifestyle, we identified numerous genes putatively involved in magnetosome biosynthesis. Remarkably, most mam orthologues were present in two paralogous copies with highest similarity to either magnetite or greigite type magnetosome genes, supporting the ability to synthesize magnetite and greigite magnetosomes.

Characterization and phylogenetic identification of a species of spherical multicellular magnetotactic prokaryotes that produces both magnetite and greigite crystals

Magnetotactic bacteria (MTB) are a group of Gram-negative bacteria synthesizing magnetic crystals that allow them aligning along magnetic field lines. They have diverse morphologies including cocci, rods, vibrio, spirilla, and multicellular magnetotactic prokaryotes (MMPs). MMPs are composed of 10–57 cells with peritrichous flagella on their outer surfaces and swim as an entire unit. Here, we describe a species of spherical MMPs isolated from intertidal sediments of Lake Yuehu (Yellow Sea, China). They were mainly found in the subsurface layer of gray-black sediments. Microscopy revealed that these spherical MMPs were 5.6 ± 0.9 μm in diameter and composed of approximately 16–32 ovoid cells with a helical arrangement and peritrichous flagellation. High-resolution transmission electron microscopy showed that the MMPs contained both bullet-shaped magnetite and irregular greigite magnetosomes that were arranged in chains or clusters. These MMPs displayed typical escape motility and negative phototaxis. The 16S rRNA genes of micromanipulation-purified spherical MMPs were cloned and sequenced. Phylogenetic analysis revealed that the MMP species was affiliated with Deltaproteobacteria and displayed >2.8% sequence divergence with respect to previously reported MMPs. This is the first phylogenetic identification of a spherical MMP that produces both magnetite and greigite magnetosomes.

A novel species of ellipsoidal multicellular magnetotactic prokaryotes from Lake Yuehu in China.

Two morphotypes of multicellular magnetotactic prokaryotes (MMPs) have been identified: spherical (several species) and ellipsoidal (previously one species). Here, we report novel ellipsoidal MMPs that are ∼ 10 × 8 μm in size, and composed of about 86 cells arranged in six to eight interlaced circles. Each MMP was composed of cells that synthesized either bullet-shaped magnetite magnetosomes alone, or both bullet-shaped magnetite and rectangular greigite magnetosomes. They showed north-seeking magnetotaxis, ping-pong motility and negative phototaxis at a velocity up to 300 μm s(-1) . During reproduction, they divided along either their long- or short-body axes. For genetic analysis, we sorted the ellipsoidal MMPs with micromanipulation and amplified their genomes using multiple displacement amplification. We sequenced the 16S rRNA gene and found 6.9% sequence divergence from that of ellipsoidal MMPs, Candidatus Magnetananas tsingtaoensis and > 8.3% divergence from those of spherical MMPs. Therefore, the novel MMPs belong to different species and genus compared with the currently known ellipsoidal and spherical MMPs respectively. The novel MMPs display a morphological cell differentiation, implying a potential division of labour. These findings provide new insights into the diversity of MMPs in general, and contribute to our understanding of the evolution of multicellularity among prokaryotes.

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

Candidatus Magnetoglobus multicellularis (Ca. M. multicellularis) is a member of a group of uncultured magnetotactic prokaryotes that possesses a unique multicellular morphology. To better understand this organism's physiology, we used a genomic approach through pyrosequencing. Genomic data analysis corroborates previous structural studies and reveals the proteins that are likely involved in multicellular morphogenesis of this microorganism. Interestingly, some detected protein sequences that might be involved in cell adhesion are homologues to phylogenetically unrelated filamentous multicellular bacteria proteins, suggesting their contribution in the early development of multicellular organization in Bacteria. Genes related to the behavior of Ca. M. multicellularis (chemo-, photo- and magnetotaxis) and its metabolic capabilities were analyzed. On the basis of the genomic-physiologic information, enrichment media were tested. One medium supported chemoorganoheterotrophic growth of Ca. M. multicellularis and allowed the microorganisms to maintain their multicellular morphology and cell cycle, confirming for the first time that the entire life cycle of the MMP occurs in a multicellular form. Because Ca. M. multicellularis has a unique multicellular life style, its cultivation is an important achievement for further studies regarding the multicellular evolution in prokaryotes.

Effect of light wavelength on motility and magnetic sensibility of the magnetotactic multicellular prokaryote ‘Candidatus Magnetoglobus multicellularis’

'Candidatus Magnetoglobus multicellularis' is a magnetotactic microorganism composed of several bacterial cells. Presently, it is the best known multicellular magnetotactic prokaryote (MMP). Recently, it has been observed that MMPs present a negative photoresponse to high intensity ultraviolet and violet-blue light. In this work, we studied the movement of 'Candidatus Magnetoglobus multicellularis' under low intensity light of different wavelengths, measuring the average velocity and the time to reorient its trajectory when the external magnetic field changes its direction (U-turn time). Our results show that the mean average velocity is higher for red light (628nm) and lower for green light (517nm) as compared to yellow (596nm) and blue (469nm) light, and the U-turn time decreased for green light illumination. The light wavelength velocity dependence can be understood as variation in flagella rotation speed, being increased by the red light and decreased by the green light relative to yellow and blue light. It is suggested that the dependence of the U-turn time on light wavelength can be considered a form of light-dependent magnetotaxis, because this time represents the magnetic sensibility of the magnetotactic microorganisms. The cellular and molecular mechanisms for this light-dependent velocity and magnetotaxis are unknown and deserve further studies to understand the biochemical interactions and the ecological roles of the different mechanisms of taxis in MMPs.

Cell Adhesion, Multicellular Morphology, and Magnetosome Distribution in the Multicellular Magnetotactic Prokaryote Candidatus Magnetoglobus multicellularis

Candidatus Magnetoglobus multicellularis is an uncultured magnetotactic multicellular prokaryote composed of 17-40 Gram-negative cells that are capable of synthesizing organelles known as magnetosomes. The magnetosomes of Ca. M. multicellularis are composed of greigite and are organized in chains that are responsible for the microorganism's orientation along magnetic field lines. The characteristics of the microorganism, including its multicellular life cycle, magnetic field orientation, and swimming behavior, and the lack of viability of individual cells detached from the whole assembly, are considered strong evidence for the existence of a unique multicellular life cycle among prokaryotes. It has been proposed that the position of each cell within the aggregate is fundamental for the maintenance of its distinctive morphology and magnetic field orientation. However, the cellular organization of the whole organism has never been studied in detail. Here, we investigated the magnetosome organization within a cell, its distribution within the microorganism, and the intercellular relationships that might be responsible for maintaining the cells in the proper position within the microorganism, which is essential for determining the magnetic properties of Ca. M. multicellularis during its life cycle. The results indicate that cellular interactions are essential for the determination of individual cell shape and the magnetic properties of the organism and are likely directly associated with the morphological changes that occur during the multicellular life cycle of this species.

Adaptation of spherical multicellular magnetotactic prokaryotes to the geochemically variable habitat of an intertidal zone

A combination of microscopic, molecular and biogeochemical methods was used to study the structure, phylogenetics and vertical distribution of spherical multicellular magnetotactic prokaryotes (MMPs) of intertidal sediments in the Yellow Sea. These MMPs were 5.5 μm in diameter and composed of approximately 15-30 cells. They synthesized bullet-shaped magnetites in chains or clusters. Phylogenetic analysis of 16S rRNA gene sequences suggested that these MMPs represent a novel species affiliated to the Deltaproteobacteria. To study their vertical distribution and the relationship to geochemical parameters, sediment cores were collected after the redox potential was measured in situ. The sediments were composed of yellow, grey and black layers from the surface to depth. The spherical MMPs were concentrated near the grey-black layer transition at a depth of 8-12 cm, while coccoid-shaped magnetotactic bacteria near the yellow-grey layer transition at a depth of 3-5 cm. The intertidal MMPs showed a deeper distribution at more reduced environments than coccoid-shaped magnetotactic bacteria, and MMPs in lagoon sediments. Additionally the MMPs were concentrated significantly in layers with high proportion of fine sand and total organic carbon, rich in leachable iron but poor in nitrate. These results show an adaptation of spherical MMPs to the peculiar intertidal sediment habitat.

Swimming behaviour of the multicellular magnetotactic prokaryote ‘Candidatus Magnetoglobus multicellularis’ under applied magnetic fields and ultraviolet light

Magnetotactic bacteria move by rotating their flagella and concomitantly are aligned to magnetic fields because they present magnetosomes, which are intracellular organelles composed by membrane-bound magnetic crystals. This results in magnetotaxis, which is swimming along magnetic field lines. Magnetotactic bacteria are morphologically diverse, including cocci, rods, spirilla and multicellular forms known as magnetotactic multicellular prokaryotes (MMPs). 'Candidatus Magnetoglobus multicellularis' is presently the best known MMP. Here we describe the helical trajectories performed by these microorganisms as they swim forward, as well as their response to UV light. We measured the radius of the trajectory, time period and translational velocity (velocity along the helix axis), which enabled the calculation of other trajectory parameters such as pitch, tangential velocity (velocity along the helix path), angular frequency, and theta angle (the angle between the helix path and the helix axis). The data revealed that 'Ca. M. multicellularis' swims along elongated helical trajectories with diameters approaching the diameter of the microorganism. In addition, we observed that 'Ca. M. multicellularis' responds to UV laser pulses by swimming backwards, returning to forward swimming several seconds after the UV laser pulse. UV light from a fluorescence microscope showed a similar effect. Thus, phototaxis is used in addition to magnetotaxis in this microorganism.

Geochemical Characteristics Related to the Gregite-Producing Multicellular Magnetotactic Prokaryote Candidatus Magnetoglobus multicellularis in a Hypersaline Lagoon

We studied the geochemical properties of sediment layers where the gregite-producing multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis exists. The ratio of iron and bioavailable sulfur concentrations regulates the population density of this microorganism. The population density can reach 8.5 × 102 cells/cm3 at an iron to sulfur ratio of 0.5. In iron- and sulfur-rich environments, microorganisms concentrated in the upper region of the oxic-anoxic zone, following an increasing nitrogen gradient with a lower isotopic 15N/14N ratio. Candidatus Magnetoglobus multicellularis prefers environmental conditions that favor the biomineralization of greigite, but in situations where the nutrient availability is low, it moves to more suitable sites.

A novel genus of multicellular magnetotactic prokaryotes from the Yellow Sea

Multicellular magnetotactic prokaryotes (MMPs) are a group of magnetotactic microorganisms composed of 10-40 Gram-negative cells. Currently, all the identified MMPs show a spherical morphology and synthesize mainly iron sulfide magnetosomes. In this study, we report a novel genus of MMPs with peculiar ellipsoidal morphology and iron oxide magnetosomes, which were discovered in intertidal sediment of the Yellow Sea in China. Optical and fluorescence microscopy revealed that this organism was ~10 × 8 µm in size and composed of ~40 cells enveloped by an outer layer. Scanning electron microscopy showed that the cells were arranged in 4-6 interlaced circles. Bullet-shaped magnetite magnetosomes were organized in chains roughly parallel to the long axis of the ellipsoidal MMPs when analysed by transmission electron microscopy. These MMPs displayed special escape motility, i.e. swimming rapidly from the edge to the centre of the droplet and then slowly back to the edge. In addition, they exhibited negative phototaxis. Light microscopy observations showed that the ellipsoidal MMPs reproduced by division along the body long axis. Both analysis of 16S rRNA gene sequence and fluorescence in situ hybridization revealed the ellipsoidal MMPs as a new genus of the Deltaproteobacteria. In summary, this novel genus of MMPs exhibit unique morphology, peculiar division process and distinct phylogenetic affiliation compared with the other MMPs.

Occurrence and microscopic analyses of multicellular magnetotactic prokaryotes from coastal sediments in the Yellow Sea

Multicellular magnetotactic prokaryotes (MMPs) are a group of aggregates composed of 7-45 gram-negative cells synthesizing intracellular magnetic crystals. Although they are thought to be globally distributed, MMPs have been observed only in marine environments in America and Europe. Most MMPs share a rosette-like morphology and biomineralize iron sulfide crystals. In the present study, abundant MMPs were observed, with a density of 26 ind./cm(3), in the sediments of a coastal lagoon, Lake Yuehu, in the Yellow Sea. Optical microscopy showed that all of them were rosette shaped with a diameter of 5.5+/-0.8 mu m. Transmission electron microscopy revealed that these MMPs were composed of 10-16 ovoid cells and flagellated peritrichously. High-resolution transmission electron microscopy and energy dispersive X-ray analysis indicated that they biomineralized bullet-shaped magnetite crystals in highly organized parallel chains within which the magnetosomes were oriented in the same direction. This is the first report of MMPs from Asia and demonstrates the ubiquitous distribution of MMPs.

Ultrastructure, tactic behaviour and potential for sulfate reduction of a novel multicellular magnetotactic prokaryote from North Sea sediments

Multicellular magnetotactic prokaryotes (MMPs) represent highly organized, spherical and motile aggregates of 10-40 bacterial cells containing magnetosomes. Although consisting of different cells, each with its own magnetosomes and flagellation, MMPs orient themselves within a magnetic field and exhibit magnetotaxis. So far, MMPs have only been found in several North and South American coastal lagoons and salt marshes. In the present study, a novel type of MMP was discovered in coastal tidal sand flats of the North Sea. High-resolution scanning electron microscopy revealed the presence of bullet-shaped magnetosomes which were aligned in several parallel chains. Within each aggregate, the magnetosome chains of individual cells were oriented in the same direction. Energy dispersive X-ray (EDX) analysis showed that the magnetosomes are composed of iron sulfide. This particular morphology and arrangement of magnetosomes has previously not been reported for other MMPs. 16S rRNA gene sequence analysis revealed a single phylotype which represented a novel phylogenetic lineage with >or= 4% sequence divergence to all previously described MMP sequences and was related to the dissimilatory sulfate-reducing Desulfosarcina variabilis within the family Desulfobacteraceae of the subphylum Deltaproteobacteria. Fluorescence in situ hybridization with a specific oligonucleotide probe revealed that all MMPs in the tidal flat sediments studied belonged to the novel phylotype. Within each MMP, all bacterial cells showed a hybridization signal, indicating that the aggregates are composed of cells of the same phylotype. Genes for dissimilatory sulfite reductase (dsrAB) and dissimilatory adenosine-5'-phosphate reductase (aprA) could be detected in purified MMP samples, suggesting that MMPs are capable of sulfate reduction. Chemotaxis assays with 41 different test compounds yielded strong responses towards acetate and propionate, whereas other organic acids, alcohols, sugars, sugar alcohols or sulfide did not elicit any response. By means of its coordinated magnetotaxis and chemotaxis, the novel type of MMP is well adapted to the steep chemical gradients which are characteristic for intertidal marine sediments.

Magnetic properties of the microorganism Candidatus Magnetoglobus multicellularis

Magnetotactic microorganisms use the interaction of internal biomineralized nanoparticles with the geomagnetic field to orientate. The movement of the magnetotactic multicellular prokaryote Candidatus Magnetoglobus multicellularis under an applied magnetic field was observed. A method using digital image processing techniques was used to track the organism trajectory to simultaneously obtain its body radius, velocity, U-turn diameter, and the reorientation time. The magnetic moment was calculated using a self-consistent method. The distribution of magnetic moments and radii present two well-characterized peaks at (9 +/- 2) x 10(-15) and (20 +/- 3) x 10(-15) A m(2) and (3.6 +/- 0.1) and (4.3 +/- 0.1) mum, respectively. For the first time, simultaneous determination of the distribution of the organism radii and magnetic moment was obtained from the U-turn method by a new digital imaging processing. The bimodal distributions support an organism reproduction process model based on electron microscopy observations. These results corroborate the prokaryote multicellular hypothesis for Candidatus M. multicellularis.

Ultrastructure and cytochemistry of lipid granules in the many-celled magnetotactic prokaryote, ‘ Candidatus Magnetoglobus multicellularis’

Conspicuous cytoplasmic granules are reported in a magnetotactic multicellular prokaryote named ‘ Candidatus Magnetoglobus multicellularis’. Unfortunately, this microorganism, which consists of an assembly of gram-negative bacterial cells, cannot yet be cultivated, limiting the biochemical analysis of the granules and preventing in vitro studies with starvation/excess of nutrients. In this scenario, light and electron microscopy techniques were used to partially address the nature of the granules. Besides magnetosomes, three types of inclusions were observed: small (mean diameter = 124 nm) polyhydroxyalkanoate-like (PHA) granules, large (diameters ranging from 0.11 to 2.5 μm) non-PHA lipid granules, and rare phosphorus-rich granules, which probably correspond to polyphosphate bodies. The PHA granules were rounded in projection, non-reactive with OsO 4, and suffered the typical plastic deformation of PHAs after freeze fracturing. The nature of the large granules, consisting of round globular structures (mean diameter = 0.76 μm), was classified as non-PHA based on the following data: (a) multilayered structure in freeze-fracture electron microscopy, typical of non-PHA lipids; (b) Nile blue fluorescence imaging detected non-PHA lipids; (c) imidazole buffered osmium tetroxide and ruthenium red cytochemistry stained the globules, which appeared as electron-dense granules instead of electron lucent as PHAs do. Most likely, ‘ Candidatus Magnetoglobus multicellularis’ stores carbon mainly as unusual lipid granules, together with smaller amounts of PHAs.

‘Candidatus Magnetoglobus multicellularis’, a multicellular, magnetotactic prokaryote from a hypersaline environment

Phylogenetic analysis and phenotypic characterization were used to assign a multicellular magnetotactic prokaryote the name 'Candidatus Magnetoglobus multicellularis'. 'Candidatus Magnetoglobus multicellularis' lives in a large hypersaline coastal lagoon from Brazil and has properties that are unique among prokaryotes. It consists of a compact assembly or aggregate of flagellated bacterial cells, highly organized in a sphere, that swim in either helical or straight trajectories. The life cycle of 'Candidatus Magnetoglobus multicellularis' is completely multicellular, in which one aggregate grows by enlarging the size of its cells and approximately doubling the volume of the whole organism. Cells then divide synchronously, maintaining the spherical arrangement; finally the cells separate into two identical aggregates. Phylogenetic 16S rRNA gene sequence analysis showed that 'Candidatus Magnetoglobus multicellularis' is related to the dissimilatory sulfate-reducing bacteria within the Deltaproteobacteria and to other previously described, but not yet well characterized, multicellular magnetotactic prokaryotes.

Magnetite (Fe 3 O 4 ) and Greigite (Fe 3 S 4 ) Crystals in Multicellular Magnetotactic Prokaryotes

Magnetotactic bacteria produce iron oxides, iron sulfides or both in organelles called magnetosomes. Most of these bacteria are unicellular and biomineralize magnetite (Fe3O4). In contrast, multicellular magnetotactic prokaryotes (MMPs) consisting of several gram-negative cells have only been known to crystallize the magnetic iron sulfide greigite (Fe3S4). In this work, we describe MMPs that mineralize magnetite in bullet-shaped crystals. Another unusual aspect is that magnetite occurs either as the only crystals or together with greigite crystals. MMPs containing only greigite in the magnetosomes occur in the same environment. These findings show that morphology, ultrastructure, and behavior are the main characteristics of the MMPs, not the type of magnetic crystal biomineralized in the magnetosomes.